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Variation and the Phylogenetic Utility of the Large Ribosomal Subunit of Mitochondrial DNA from the Insect Order Hymenoptera JAMES N

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Variation and the Phylogenetic Utility of the Large Ribosomal Subunit of Mitochondrial DNA from the Insect Order Hymenoptera JAMES N MOLECULAR PHYLOGENETICS AND EVOLUTION Vol. 1, No. 2, June, pp. 136-147, 1992 Variation and the Phylogenetic Utility of the Large Ribosomal Subunit of Mitochondrial DNA from the Insect Order Hymenoptera JAMES N. DERR,* SCOTT K. DAVIS,* JAMES B. WooLLEY,t AND ROBERT A. Wwmord *Department of Animal Sciences and tDepartment of Entomology, Texas A&M University, College Station, Texas 77843 Received February 4, 1992; revised July 6, 1992 provide pivotal information for investigating these Nucleotide sequence variation from a 573-bp region questions. Nevertheless, clearly supported and robust of the mitochondrial 16s rRNA gene was determined models of the phylogenetic relationships for major com- for representative hymenopteran taxa. An overall bias ponents of the Hymenoptera are lacking. in the distribution of A and T bases was observed from The most recent and comprehensive investigations all taxa; however, the terebrants (parasitoids) dis- regarding hymenopteran phylogeny are those of Ks- played significantly lower AT ratios as well as a higher nigsmann (1976, 1977, 1978a,b) and Rasnitsyn (1980, degree of strand asymmetry. Moreover, a strong posi- 1988). A number of other recent investigations have tive correlation was observed between relative AT rich- examined either specific superfamilies within the Hy- ness and sequence divergence, suggesting selection at menoptera (Brothers, 1975; Carpenter, 1986; Gibson, the nucleotide level for A and T bases as well as func- 1986) or various character systems across taxa (e.g., tionality. Overall sequence difference ranged from 2.3 Saini and Dhillon, 1980; Gibson, 1985; Darling, 1988; to 53.4%, with the maximum divergence between mem- Johnson, 1988; Whitfield et al., 1989). While these bers of the two Hymenopteran suborders. These data were used in a phylogenetic analysis to illustrate the studies have generally increased our understanding of utility and degree of resolution provided by this infor- the morphological basis for interpreting relationships, mation at various hierarchical levels within this taxo- there is nonetheless little congruence among research- nomically diverse order. Parsimony analysis revealed ers regarding higher classification. strong evidence for monophyly of the aculeates and the Composition of the Symphyta varies depending on terebrants. Most noteworthy was a strongly supported whether the Cephidae (Kanigsmann, 1977) or the Orus- clade containing the two terebrant superfamilies Icheu- sidae (Rasnitsyn, 1980) are removed and placed as the monoidea and Chalcidoidea. Conversely, high se- sister group to the Apocrita. Even when both are re- quence divergence values resulted in instability at the tained in the Symphyta (the traditional arrangement), base of the tree and limited resolution at the higher there are problems in establishing a symphytan lin- taxonomic levels. Nevertheless, these results do identify eage based on shared, derived features relative to the those taxonomic levels for which 16s rRNA sequences Apocrita (Gibson, 1986; Gauld and Bolton, 1988; John- are phylogenetically informative. 8 1892 Academic PWIS, hc. son, 1988) and the group is now widely regarded as paraphyletic (Gauld and Bolton, 1988). More detailed resolution of the Symphyta is crucial for understand- ing the origins of the Apocrita and in particular for establishing character polarities within Apocrita using INTRODUCTION outgroup arguments. The Apocrita are generally interpreted as monophy- The Hymenoptera is one of the more diverse and letic largely on the basis of the fusion of the first ab thoroughly studied insect orders. Traditionally, this dominal segment to the thorax. It is usually subdivided order is divided into two suborders, Symphyta and into the Aculeata and the Terebrantes (Parasitical. Apocrita, that together contain some 110,000 described The aculeate Hymenoptera (ants, solitary and social species. The Symphyta is composed ofthe sawflies, horn- wasps, and bees) almost certainly form a monophyletic tails, and parasitic wood wasps, whereas the Apocrita group (Brothers, 1975; Carpenter, 1986); however, se- contains the majority of the parasitic Hymenoptera, rious questions remain regarding the monophyly of the the ants, solitary and social wasps, and bees. The evo- terebrants (“parasitoids”) due to the lack of demon- lution of parasitism and social behavior in this order strated synapomorphies. has generated considerable interest, and recently Car- The parasitoids belong to at least nine currently rec- penter (1989) proposed that phylogenetic methods may ognized superfamilies whose relationships and compo- 136 1055-7903/92 $5.00 Copyright 0 1992 by Academic Press, Inc. All rights of reproduction in any form reserved. mtDNA 16s I-RNA SEQUENCE VARIATION FROM HYMENOPTERA 137 sition are the subject of some debate (Konigsmann, DNA Amplification 1978a; Rasnitsyn, 1980, 1988; Naumann and Masner, 1985; Gibson, 1986; Gauld and Bolton, 1988). Of partic- At the time we initiated this study, few oligonucleo- ular interest here is the recent suggestion that the tide primers were available for amplified specific DNA Aculeata and the terebrant superfamily Ichneumo- sequences from insect taxa. We used an edited version noidea (Ichneumonidae -t- Braconidae) are sister of the primers first designed by T. Kocher (personal groups (Rasnitsyn, 1988; Mason, unpublished obser- communication) to amplify a region of the 16s rRNA vation). gene. These primers were chosen because they pro- Two attributes of the order Hymenoptera make it duced consistent PCR products from a number of differ- particularly appealing for investigations using molec- ent hymenopteran taxa. Primer sequences are repre- ular techniques. First, although a number of morpho- sented by the light (L) or heavy (H) strand of mtDNA logical-based studies are available for various groups and their position relative to the complete Drosophila within this order, few provide well-supported phyloge- mtDNA sequence (Clary and Wolstenholme, 1985). netic hypotheses. For example, many of these studies Both primers were constructed with 5’ terminal EcoRI are not based on sound phylogenetic methods and even restriction enzyme sites plus one additional base to fa- when they are, reductional features (such as loss of cilitate plasmid cloning of the amplified products. The wing veins), which are commonplace throughout the sequences of these two primers are as follows: primer order, often confuse attempts to assess character ho- 16saEcoRI (L-12,883), 5’-GGAATTCCCTCCGG’ITTG- mology. In addition, lack of agreement on even funda- AACTCAGATC-3’; and primer 16sbEcoRI (H-13,398), mental relationships hinders the interpretation of 5’-GGAA’Il’CCCGCCTG’ITI’ATCAAAAACAT-3’. Sub- character polarity. Second, the very small size of many sequently, “nested” primers were developed based on of the parasitic wasps (many Cl mm) prevents a molec- our initial sequence in comparison with the published ular genetic evaluation due to the lack of sufficient 16s rRNA sequences from Drosophila (Clary and Wol- material. However, techniques such as polymerase stenholme, 1985), Aeoks (Hsu-Chen et al., 19841, and chain reaction (PCR) offer new and powerful tools that Apis (Vlasak et al., 1987). The sequences of these prim- promise to provide new information that will greatly ers are 16saW (L-12,943),5’-TAATAATCAAACATA- facilitate future systematic research on this group of GAGGTCG-3’; and 16sbW (H-13,332), 5’-GACTGTT- insects. CAAAGGTAGCATAAT-3’. In this study we use PCR to illuminate DNA se- Template DNAs were amplified in 50 or 100~p,l total quence variation from the large ribosomal subunit reaction volumes with 30-35 PCR cycles (Saiki et al., (16s rRNA) of the mitochondrial genome from mem- 1988). Most primer/template combinations were am- bers of six superfamilies representing both suborders plified using the thermal stable DNA polymerase Taq (Symphyta and Apocrita) of Hymenoptera. These data (International Biotechnologies, Inc.) although Vent are used in a phylogenetic analysis to illustrate the DNA polymerase (New England BioLabs) was also utility and degree of resolution provided by this infor- used. All amplifications were performed with a Perkin mation at various hierarchical levels within this taxo- Elmer-Cetus thermal cycler with the following proto- nomically diverse order. For comprehensive reviews of col: 35 cycles of DNA denaturing at 93°C for 30 s, the utility of mitochondrial DNA (mtDNA) for evolu- primer annealing at 42-50°C for 60 s, and primer ex- tionary studies see the work of Moritz et al. (1987) and tension at 72°C for 2 min. With some template/primer Harrison (1989). combinations the insertion of a 4-min step cycle be- tween annealing and extension increased the yield of the final amplification product. One explanation may METHODS AND MATERIALS be the rapid stabilization of partially mismatched primer/template complexes by the DNA polymerase as DNA Extraction and Purification the reaction slowly warms from the annealing temper- DNA was extracted from frozen ( - SO’C) or ethanol- ature to (42-50°C) to the extension temperature preserved specimens using the proteinase K digestion (72°C). protocol of Maniatis et al. (1982). Final DNA pellets Following PCR, the amplified products were sepa- were washed in ice-cold 70% ethanol, redissolved in rated by electrophoresis in 1.5% agarose minigels (Ma- sterile water, and stored at 4°C. From the small-bodied niatis et al., 1982). Gels were stained with ethidium parasitic species, DNA was isolated following whole-
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